Tokyo Godfathers tells the story of three homeless people; Gin, an alcoholic and middle-aged hobo; Hana, a transgender woman and former drag queen; Miyuki, a runaway teenage girl, and the baby girl they find one Christmas Eve. The three take it upon themselves to return the baby to her parents, all while slowly coming to confront past and present regrets.

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On a Christmas Eve, three of Tokyo's homeless: high school runaway Miyuki; middle-aged alcoholic, Gin; and ex drag queen transgender woman Hana, stumble upon a crying baby place within a pile of garbage. The three take in the baby and go on fantastic adventure in search of the baby's mother. Along the way getting involved with mafia dons, an assassination attempt, a suicidal woman, and a crazy car chase.

On Christmas Eve, after a nativity service for the homeless of Tokyo, Hana takes the other two to help her find Miyuki's present, which she hid in a dumpster. Gin and Miyuki get into a fight, but then they stop when they hear a baby crying, and discover a new-born among the trash. Hana, a drag-queen believes the baby is a gift from God, as she wanted to be a mother, but Gin informs that they must return the baby to her parents. Hana agrees and they discover clues from a baby-bag filled with baby food, such as a photograph of a couple and a locker key. Hana decides to name the baby girl Kiyoko, meaning "pure child", as Christmas Eve is the purest of all nights.

They take Kiyoko to their tent and Hana sends Miyuki to run an errand. Gin then tells Hana that he once had a daughter, but she fell ill, and Gin had no money for medicine. A con man helped him in a scheme to get the money by throwing a bicycle race, but the scandal was discovered, and Gin's daughter and wife died later, leaving Gin to succumb to alcoholism.

The next day, the group heads to the train station, where they use the locker key's number to find the locker. In it, they find a set of house keys and a club's phone number, but they can't get a hold of the owner. They board a light train, but Miyuki escapes after she spots her father in another train, spillng the baby food in the process. Gin and Hana, with Kiyoko in her arms, go after Miyuki, and they begin to wander in the streets, as it begins to snow. Kiyoko becomes hungry and begins to cry, so the group begins to look for something to eat. They go into a graveyard, where they find an offering of baby supplies, convincing Hana that Kiyoko is favored by God. Outside the graveyard, they find a high-ranking yakuza man ( Japanese mafia), trapped under his car. They free him and he asks what he can do to thank them. They ask about the address of the club on the card and where to find the owner. He takes them to the club, where his daughter (also named Kiyoko) is getting married to the owner. The group help themselves to food and drinks, while the yakuza searches for his son-in-law. Kiyoko the baby begins to cry and Miyuki takes her to change her diaper. Gin is then shocked to see the groom, informing Hana that he is the con man who set up the bicycle race scandal.

The groom informs the two about Sachiko, the woman in the picture, who used to work at the club. He offers them Sachiko's address, but the party is interrupted by a maid, who is revealed to be a Hispanic hit-man in disguise. He attends to shoot the yakuza, but the groom takes the shots. The hit-man runs off, taking Miyuki and Kiyoko the baby as hostages and they flee into a taxi. The hit-man takes them to his home, where they meet his wife, who is much kinder and warm-hearted and also has a baby. She breast-feeds Kiyoko along with her child, while she and Miyuki get acquainted, despite a language-barrier. Miyuki shows the wife some pictures of her family including her policeman father, religious mother, and her cat, Angel. Miyuki begins to cry and tells the wife that she ran away from home after stabbing her father, believing that he got rid of Angel.

Meanwhile, Hana calls the taxi service about the abduction, and they sent the cab driver who took the hit-man. Gin, however, wants to call the police, but Hana wants to find the kidnapped girls. Gin walks off, leaving Hana to find the girls. Awhile later, he finds an elderly homeless man, dying and Gin takes him to his tent, where he dies peacefully. Gin then notices a picture of two buildings and compares it to the photo of the couple, the backgrounds matching. Then, some teenagers show up and attack Gin and the deceased homeless man, and trash the place as a form of "clean-up". Gin is badly wounded and wanders through the streets, looking for Hana.

The cab driver brings Hana to the hit-man's place and Hana runs down the alley, but stops and coughs up blood. She then finds the girls safe and sound. They thank the Hispanic woman and leave to find a place to spend the night. Then, they hear a group of paramedics informing about the deceased homeless man, and they believe it's Gin. Hana cuddles the body, only to find out that it is the elderly man. Gin is then rescued by an "angel", a woman who is really dressed up as one.

Hana takes the two girls to a club where she used to work at and introduces her "mother" (another drag queen who raised her). They also find Gin there, beaten up, but well-taken care of. Hana and her "mother" talk about the death of Hana's boyfriend, and how Hana left the club after attacking an especially rude customer. She then informs her mother about the baby, Kiyoko and her "mother" encourages her to keep looking for the parents. While doing laundry, Hana sees the photo of the two buildings and immediately recognizes it.

The group takes a train to another part of Tokyo, where the two buildings are. A snow storm forces them to take shelter at an empty construction site. Awhile later, Miyuki goes to run an errand, only to be stopped when she sees a demolished house with the two buildings in the background. Gin checks the house keys, which they work at a lone standing door. The next morning, the group asks the neighbors of what they know of Sachiko, while Miyuki looks around the wreckage for anything useful, and she finds a newspaper, with her in the missing persons section. Her father wants her to come home and informs her that Angel came back. The neighbors explain that Sachiko's marriage was rocky and she and her husband would fight all the time. They eventually went into debt because of the husband's gambling and alcoholism and they were forced to leave the house.

That evening, Gin and Hana, with Kiyoko stop to rest at a store, but they get into an argument with a drunken man. Miyuki goes to call her father, but she is too scared to talk to him. She returns to find the group fighting with the drunken man outside. Suddenly, a run-away ambulance crashes into the store and Hana prasies to God for saving them, she then collapses and coughs up blood.

Hana is taken to the hospital and Gin talks to the physician, who advises that Hana should get some rest. Gin explains that they are homeless, but the physician says he deals with all kinds of people, even the homeless. In the lobby, Miyuki meets Kiyoko the nurse and she is surprised to see Gin, her father. The two join in conversation; the truth is revealed that Gin once owned a bicycle shop, but he left his family when his gambling and alcoholism got worse and the con-man was really someone Gin owed money to. Hana becomes angry, realizing that everything that Gin said to her before was a lie and she insults Gin in front of his daughter, then she and Miyuki, with the baby leave Gin.

Miyuki asks Hana if insulting Gin in front of his daughter was the right thing, although Hana thinks she will forgive him. She then tells the story of "The Weeping Red Devil"; the red devil was feared by the villagers, but he wanted to be friends with them. His friend, the blue devil thought up a plan, he would wreck havoc on the village and the red devil would save them. The plan worked, but the blue devil had to go away, in order to prevent the villagers from believing it was a trick. Miyuki is shocked to hear that Hana plans to leave the group once they find Sachiko. Back at the hospital, Gin sees a report about a kidnapped baby, who looks exactly like Kiyoko the baby.

Hana and Miyuki then rescue a woman from committing suicide and realize it's Sachiko. She informs them that her husband took Kiyoko while she was out and fell into deperssion. Hana gives Kiyoko back to Sachiko, but the baby cries continuously. Elsewhere, Gin finds an apartment and goes into one complex, that is filled with trash and unopened mail. He finds Sachiko's husband amoung the clutter and angrily bellows at him for being a horrible father, but the husband informs that the baby is not his, nor is Sachiko's. He replies that Sachiko stole the baby and he hid her in hopes that the police would find her, although Gin calls him a terrible person, for he didn't do the right thing. Gin takes a bicycle and goes to look for Hana and Miyuki.

At the temple, everyone, including Hana and Miyuki pay their respects for the new year. Gin arrives to inform them what he learned from the husband and they head off to find Sachiko. They go on a wild goose chase, when Sachiko steals a delivery truck and Gin steals a policeman's bicycle and goes after the truck. Hana stops a taxi and the driver recongizes her and they go after them. Gin grabs onto the passenger door and Sachiko crashes the truck into a building. She then takes Kiyoko and heads to the rooftop, with Miyuki in pursuit. Sachiko threatens to committ suicide with Kiyoko, stopping Miyuki in her tracks. Sachiko's husband sees his wife on the news and realizes what he has done to her and to himself. Miyuki asks why Sachiko stole Kiyoko. Sachiko explains that she lost her own baby in a miscarriage and took Kiyoko as a replacement. Miyuki informs that life is born once and people are responsible for their futures. She encourages Sachiko to give Kiyoko back, but she is about to jump off, when her husband calls out to her, informing her that they can start over. Miyuki catches Sachiko as she steps off, informing her that Kiyoko wants to go back to her parents, and Sachiko surrenders. Miyuki begins to slip, but Gin catches them, but Sachiko accidently drops Kiyoko. In a daring attempt, Hana runs down the side and catches Kiyoko, but she slips and catches a banner. The banner breaks away, sending both of them towards earth, but a strong wind fills the banner and floats Hana with Kiyoko in her arms down to the ground safe and sound.

Awhile later, Kiyoko is reunited with her real parents and the group is treated at the hospital. The parents want to thank them and want them to be Kiyoko's godparents, so the police inspector in charge of finding Kiyoko lets them in and is extremely surprised to see Miyuki. She stares back at him and whispers "Dad."

There are numerous references of the "12-25 (Christmas)" date, such as: the locker key number, the cab fare, the address in the newspaper ad, the cab license plate, the alarm clock in Sachiko's demolished house, etc.

Towards the beginning of the movie, the group passes a bus stop, in the background you can see theatrical posters for 'Perfect Blue' and 'Millennium Actress', both directed by Satoshi Kon.